Role of capsaicin-sensitive C-fiber afferents in neuropathic pain-induced synaptic potentiation in the nociceptive amygdala

详细信息    查看全文

• 作者：Ayano Nakao (1)
  Yukari Takahashi (1)
  Masashi Nagase (1)
  Ryo Ikeda (2)
  Fusao Kato (1) (3)
  
• 关键词：Excitatory postsynaptic currents ; Parabrachial nucleus ; Tactile allodynia ; Emotion ; Minimal stimulation ; Capsular part of the central nucleus of the amygdala
• 刊名：Molecular Pain
• 出版年：2012
• 出版时间：December 2012
• 年：2012
• 卷：8
• 期：1
• 全文大小：424KB
• 参考文献：1. Kobayakawa K, Kobayakawa R, Matsumoto H, Oka Y, Imai T, Ikawa M, Okabe M, Ikeda T, Itohara S, Kikusui T, / et al.: Innate versus learned odour processing in the mouse olfactory bulb. / Nature 2007, 450:503鈥?08. CrossRef
  2. Fontanini A, Grossman SE, Figueroa JA, Katz DB: Distinct subtypes of basolateral amygdala taste neurons reflect palatability and reward. / J Neurosci 2009, 29:2486鈥?495. CrossRef
  3. Darwin C, Darwin F: / The Expression of the Emotions in Man and Animals. 2nd edition. Cambridge University Press, London; 2009. CrossRef
  4. Meyerhof W: Elucidation of mammalian bitter taste. / Rev Physiol Biochem Pharmacol 2005, 154:37鈥?2. CrossRef
  5. Todd AJ: Neuronal circuitry for pain processing in the dorsal horn. / Nat Rev Neurosci 2010, 11:823鈥?36. CrossRef
  6. Todd AJ, Puskar Z, Spike RC, Hughes C, Watt C, Forrest L: Projection neurons in lamina I of rat spinal cord with the neurokinin 1 receptor are selectively innervated by substance p-containing afferents and respond to noxious stimulation. / J Neurosci 2002, 22:4103鈥?113.
  7. Gauriau C, Bernard JF: Pain pathways and parabrachial circuits in the rat. / Exp Physiol 2002, 87:251鈥?58. CrossRef
  8. Sarhan M, Freund-Mercier MJ, Veinante P: Branching patterns of parabrachial neurons projecting to the central extended amgydala: single axonal reconstructions. / J Comp Neurol 2005, 491:418鈥?42. CrossRef
  9. Dong YL, Fukazawa Y, Wang W, Kamasawa N, Shigemoto R: Differential postsynaptic compartments in the laterocapsular division of the central nucleus of amygdala for afferents from the parabrachial nucleus and the basolateral nucleus in the rat. / J Comp Neurol 2010, 518:4771鈥?791. CrossRef
  10. Paxinos G, Watson C: / The Rat Brain in Stereotaxic Coordinates. Sixth Edition, Academic Press; 2008.
  11. Neugebauer V, Li WD, Bird GC, Han JS: The amygdala and persistent pain. / Neuroscientist 2004, 10:221鈥?34. CrossRef
  12. Ehrlich I, Humeau Y, Grenier F, Ciocchi S, Herry C, Luthi A: Amygdala inhibitory circuits and the control of fear memory. / Neuron 2009, 62:757鈥?71. CrossRef
  13. Neugebauer V, Galhardo V, Maione S, Mackey SC: Forebrain pain mechanisms. / Brain Res Rev 2009, 60:226鈥?42. CrossRef
  14. Cheng SJ, Chen CC, Yang HW, Chang YT, Bai SW, Yen CT, Min MY: Role of extracellular signal-regulated kinase in synaptic transmission and plasticity of a nociceptive input on capsular central amygdaloid neurons in normal and acid-induced muscle pain mice. / J Neurosci 2011, 31:2258鈥?270. CrossRef
  15. Ikeda R, Takahashi Y, Inoue K, Kato F: NMDA receptor-independent synaptic plasticity in the central amygdala in the rat model of neuropathic pain. / Pain 2007, 127:161鈥?72. CrossRef
  16. Kim SH, Chung JM: An experimental model for peripheral neuropathy produced by segmental spinal nerve ligation in the rat. / Pain 1992, 50:355鈥?63. CrossRef
  17. Ossipov MH, Bian D, Malan TP, Lai J, Porreca F: Lack of involvement of capsaicin-sensitive primary afferents in nerve-ligation injury induced tactile allodynia in rats. / Pain 1999, 79:127鈥?33. CrossRef
  18. Nagy JI, Iversen LL, Goedert M, Chapman D, Hunt SP: Dose-dependent effects of capsaicin on primary sensory neurons in the neonatal rat. / J Neurosci 1983, 3:399鈥?06.
  19. Holzer P, Jurna I, Gamse R, Lembeck F: Nociceptive threshold after neonatal capsaicin treatment. / Eur J Pharmacol 1979, 58:511鈥?14. CrossRef
  20. Faulkner DC, Growcott JW: Effects of neonatal capsaicin administration on the nociceptive response of the rat to mechanical and chemical stimuli. / J Pharm Pharmacol 1980, 32:656鈥?57. CrossRef
  21. Nagy JI, Vincent SR, Staines WA, Fibiger HC, Reisine TD, Yamamura HI: Neurotoxic action of capsaicin on spinal substance P neurons. / Brain Res 1980, 186:435鈥?44. CrossRef
  22. Fu Y, Han J, Ishola T, Scerbo M, Adwanikar H, Ramsey C, Neugebauer V: PKA and ERK, but not PKC, in the amygdala contribute to pain-related synaptic plasticity and behavior. / Mol Pain 2008, 4:26. CrossRef
  23. Jancso G, Kiraly E: Sensory neurotoxins: chemically induced selective destruction of primary sensory neurons. / Brain Res 1981, 210:83鈥?9. CrossRef
  24. Hao JX, Yu W, Xu XJ, Wiesenfeld-Hallin Z: Capsaicin-sensitive afferents mediate chronic cold, but not mechanical, allodynia-like behavior in spinally injured rats. / Brain Res 1996, 722:177鈥?80. CrossRef
  25. Yamamoto K, Noguchi J, Yamada C, Watabe AM, Kato F: Distinct target cell-dependent forms of short-term plasticity of the central visceral afferent synapses of the rat. / BMC Neurosci 2010, 11:134. CrossRef
  26. Jancso G, Kiraly E, Jancso-Gabor A: Pharmacologically induced selective degeneration of chemosensitive primary sensory neurones. / Nature 1977, 270:741鈥?43. CrossRef
  27. Nagy JI, Hunt SP, Iversen LL, Emson PC: Biochemical and anatomical observations on the degeneration of peptide-containing primary afferent neurons after neonatal capsaicin. / Neuroscience 1981, 6:1923鈥?934. CrossRef
  28. Arvidsson J, Ygge J: A quantitative study of the effects of neonatal capsaicin treatment and of subsequent peripheral nerve transection in the adult rat. / Brain Res 1986, 397:130鈥?36. CrossRef
  29. Woolf CJ, Doubell TP: The pathophysiology of chronic pain - increased sensitivity to low threshold A beta-fibre inputs. / Curr Opin Neurobiol 1994, 4:525鈥?34. CrossRef
  30. Sandkuhler J: Models and mechanisms of hyperalgesia and allodynia. / Physiol Rev 2009, 89:707鈥?58. CrossRef
  31. Seal RP, Wang X, Guan Y, Raja SN, Woodbury CJ, Basbaum AI, Edwards RH: Injury-induced mechanical hypersensitivity requires C-low threshold mechanoreceptors. / Nature 2009, 462:651鈥?55. CrossRef
  32. Szallasi A, Joo F, Blumberg PM: Duration of desensitization and ultrastructural changes in dorsal root ganglia in rats treated with resiniferatoxin, an ultrapotent capsaicin analog. / Brain Res 1989, 503:68鈥?2. CrossRef
  33. Caterina MJ, Leffler A, Malmberg AB, Martin WJ, Trafton J, Petersen-Zeitz KR, Koltzenburg M, Basbaum AI, Julius D: Impaired nociception and pain sensation in mice lacking the capsaicin receptor. / Science 2000, 288:306鈥?13. CrossRef
  34. Guo A, Simone DA, Stone LS, Fairbanks CA, Wang J, Elde R: Developmental shift of vanilloid receptor 1 (VR1) terminals into deeper regions of the superficial dorsal horn: correlation with a shift from TrkA to Ret expression by dorsal root ganglion neurons. / Eur J Neurosci 2001, 14:293鈥?04. CrossRef
  35. Lu CR, Hwang SJ, Phend KD, Rustioni A, Valtschanoff JG: Primary afferent terminals that express presynaptic NR1 in rats are mainly from myelinated, mechanosensitive fibers. / J Comp Neurol 2003, 460:191鈥?02. CrossRef
  36. Al-Khater KM, Todd AJ: Collateral projections of neurons in laminae I, III, and IV of rat spinal cord to thalamus, periaqueductal gray matter, and lateral parabrachial area. / J Comp Neurol 2009, 515:629鈥?46. CrossRef
  37. Shortland P, Kinnman E, Molander C: Sprouting of A-fibre primary afferents into lamina II in two rat models of neuropathic pain (vol 1, pg 215, 1997). / Eur J Pain London 1998, 2:91鈥?1. CrossRef
  38. Woolf CJ, Shortland P, Coggeshall RE: Peripheral nerve injury triggers central sprouting of myelinated afferents. / Nature 1992, 355:75鈥?8. CrossRef
  39. Wu G, Ringkamp M, Hartke TV, Murinson BB, Campbell JN, Griffin JW, Meyer RA: Early onset of spontaneous activity in uninjured C-fiber nociceptors after injury to neighboring nerve fibers. / J Neurosci 2001, 21:RC140.
  40. Fukuoka T, Noguchi K: Contribution of the spared primary afferent neurons to the pathomechanisms of neuropathic pain. / Mol Neurobiol 2002, 26:57鈥?7. CrossRef
  41. Keller AF, Beggs S, Salter MW, De Koninck Y: Transformation of the output of spinal lamina I neurons after nerve injury and microglia stimulation underlying neuropathic pain. / Mol Pain 2007, 3:27. CrossRef
  42. Cortright DN, Crandall M, Sanchez JF, Zou T, Krause JE, White G: The tissue distribution and functional characterization of human VR1. / Biochem Biophys Res Commun 2001, 281:1183鈥?189. CrossRef
  43. Toth A, Boczan J, Kedei N, Lizanecz E, Bagi Z, Papp Z, Edes I, Csiba L, Blumberg PM: Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. / Brain Res Mol Brain Res 2005, 135:162鈥?68. CrossRef
  44. Szabo T, Biro T, Gonzalez AF, Palkovits M, Blumberg PM: Pharmacological characterization of vanilloid receptor located in the brain. / Brain Res Mol Brain Res 2002, 98:51鈥?7. CrossRef
  45. Sanchez JF, Krause JE, Cortright DN: The distribution and regulation of vanilloid receptor VR1 and VR1 5' splice variant RNA expression in rat. / Neuroscience 2001, 107:373鈥?81. CrossRef
  46. Hori T, Tsuzuki S: Thermoregulation in adult rats which have been treated with capsaicin as neonates. / Pflugers Arch 1981, 390:219鈥?23. CrossRef
  47. Zschenderlein C, Gebhardt C, von Bohlen Und Halbach O, Kulisch C, Albrecht D: Capsaicin-Induced Changes in LTP in the Lateral Amygdala Are Mediated by TRPV1. / PLoS One 2011, 6:e16116. CrossRef
  48. Beggs S, Liu XJ, Kwan C, Salter MW: Peripheral nerve injury and TRPV1-expressing primary afferent C-fibers cause opening of the blood鈥揵rain barrier. / Mol Pain 2010, 6:74. CrossRef
  49. Price DD: Psychological and neural mechanisms of the affective dimension of pain. / Science 2000, 288:1769鈥?772. CrossRef
  50. Fontanini A, Katz DB: State-dependent modulation of time-varying gustatory responses. / J Neurophysiol 2006, 96:3183鈥?193. CrossRef
  51. Zimmermann M: Ethical guidelines for investigations of experimental pain in conscious animals. / Pain 1983, 16:109鈥?10. CrossRef
  52. Jancso G, Kiraly E, Jancso-Gabor A: Direct evidence for an axonal site of action of capsaicin. / Naunyn Schmiedebergs Arch Pharmacol 1980, 313:91鈥?4. CrossRef
  53. Gamse R, Lackner D, Gamse G, Leeman SE: Effect of capsaicin pretreatment on capsaicin-evoked release of immunoreactive somatostatin and substance P from primary sensory neurons. / Naunyn Schmiedebergs Arch Pharmacol 1981, 316:38鈥?1. CrossRef
  54. Welk E, Fleischer E, Petsche U, Handwerker HO: Afferent C-fibres in rats after neonatal capsaicin treatment. / Pflugers Arch 1984, 400:66鈥?1. CrossRef
  55. Chaplan SR, Bach FW, Pogrel JW, Chung JM, Yaksh TL: Quantitative assessment of tactile allodynia in the rat paw. / J Neurosci Methods 1994, 53:55鈥?3. CrossRef
  56. Raastad M, Storm JF, Andersen P: Putative Single Quantum and Single Fibre Excitatory Postsynaptic Currents Show Similar Amplitude Range and Variability in Rat Hippocampal Slices. / Eur J Neurosci 1992, 4:113鈥?17. CrossRef
  
• 作者单位：Ayano Nakao (1)
  Yukari Takahashi (1)
  Masashi Nagase (1)
  Ryo Ikeda (2)
  Fusao Kato (1) (3)
  
  1. Laboratory of Neurophysiology, Department of Neuroscience, Jikei University School of Medicine, Minato-ku, Tokyo, 105-8461, Japan
  2. Department of Orthopaedics, Jikei University School of Medicine, Minato-ku, Tokyo, 105-8461, Japan
  3. Nagoya University Graduate School of Medicine, Department of Cell Pharmacology, Graduate School of Medicine, Nagoya University, 65 Tsurumai, Showa, Nagoya, Aichi, 466-8550, Japan
  

文摘

Background Neurons in the capsular part of the central nucleus of the amygdala (CeC), a region also called "nociceptive amygdala," receive nociceptive information from the dorsal horn via afferent pathways relayed from the lateral parabrachial nucleus (LPB). As the central amygdala is known to be involved in the acquisition and expression of emotion, this pathway is thought to play central roles in the generation of affective responses to nociceptive inputs. Excitatory synaptic transmission between afferents arising from the LPB and these CeC neurons is potentiated in arthritic, visceral, neuropathic, inflammatory and muscle pain models. In neuropathic pain models following spinal nerve ligation (SNL), in which we previously showed a robust LPB-CeC potentiation, the principal behavioral symptom is tactile allodynia triggered by non-C-fiber low-threshold mechanoreceptor afferents. Conversely, recent anatomical studies have revealed that most of the spinal neurons projecting to the LPB receive C-fiber afferent inputs. Here, we examined the hypothesis that these C-fiber-mediated inputs are necessary for the full establishment of robust synaptic potentiation of LPB-CeC transmission in the rats with neuropathic pain. Results Postnatal capsaicin treatment, which has been shown to denervate the C-fibers expressing transient receptor potential vanilloid type-1 (TRPV1) channels, completely abolished eye-wiping responses to capsaicin eye instillation in rats, but this treatment did not affect mechanical allodynia in the nerve-ligated animals. However, the postnatal capsaicin treatment prevented LPB-CeC synaptic potentiation after SNL, unlike in the vehicle-treated rats, primarily due to the decreased incidence of potentiated transmission by elimination of TRPV1-expressing C-fiber afferents. Conclusions C-fiber-mediated afferents in the nerve-ligated animals may be a required facilitator of the establishment of nerve injury-evoked synaptic potentiation in the CeC. These inputs might play essential roles in the chronic pain-induced plastic changes in the central network linking nociception and negative emotion.